Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.psychology | behavior | comparative methods | inhibitory control | executive function S ince Darwin, understanding the evolution of cognition has been widely regarded as one of the greatest challenges for evolutionary research (1). Although researchers have identified surprising cognitive flexibility in a range of species (2-40) and potentially derived features of human psychology (41-61), we know much less about the major forces shaping cognitive evolution (62-71). With the notable exception of Bitterman's landmark studies conducted several decades ago (63, 72-74), most research comparing cognition across species has been limited to small taxonomic samples (70, 75). With limited comparable experimental data on how cognition varies across species, previous research has largely relied on proxies for cognition (e.g., brain size) or metaanalyses when testing hypotheses about cognitive evolution (76-92). The lack of cognitive data collected with similar methods across large samples of species precludes meaningful species comparisons that can reveal the major forces shaping cognitive evolution across species, including humans (48,70,89,(93)(94)(95)(96)(97)(98). SignificanceAlthough scientists have identified surprising cognitive flexibility in animals and potentially unique features of human psychology, we know less about the selective forces that favor cognitive evolution, or the proximate biological mechanisms underlying this process. We tested 36 species in two problemsolving tasks measuring self-control and evaluated the leading hypotheses regarding how ...

The Machiavellian Intelligence or Social Brain Hypothesis explains the evolution of increased brain size as mainly driven by living in complex organized social systems in which individuals represent "moving targets" who can adopt multiple strategies to respond to one another. Frequently splitting and merging in subgroups of variable composition (fission-fusion or FF dynamics) has been proposed as one aspect of social complexity ( compare with) that may be associated with an enhancement of cognitive skills like inhibition, which allows the suppression of prepotent but ineffective responses in a changing social environment. We compared the performance of primates experiencing high levels of FF dynamics (chimpanzees, bonobos, orangutans, and spider monkeys) to that of species living in more cohesive groups (gorillas, capuchin monkeys, and long-tailed macaques) on five inhibition tasks. Testing species differing in diet, phylogenetic relatedness, and levels of FF dynamics allowed us to contrast ecological, phylogenetic, and socioecological explanations for interspecific differences. Spider monkeys performed at levels comparable to chimpanzees, bonobos, and orangutans, and better than gorillas. A two-cluster analysis grouped all species with higher levels of FF dynamics together. These findings confirmed that enhanced inhibitory skills are positively associated with FF dynamics, more than to phylogenetic relations or feeding ecology.

Proactive, that is, unsolicited, prosociality is a key component of our hyper-cooperation, which in turn has enabled the emergence of various uniquely human traits, including complex cognition, morality and cumulative culture and technology. However, the evolutionary foundation of the human prosocial sentiment remains poorly understood, largely because primate data from numerous, often incommensurable testing paradigms do not provide an adequate basis for formal tests of the various functional hypotheses. We therefore present the results of standardized prosociality experiments in 24 groups of 15 primate species, including humans. Extensive allomaternal care is by far the best predictor of interspecific variation in proactive prosociality. Proactive prosocial motivations therefore systematically arise whenever selection favours the evolution of cooperative breeding. Because the human data fit this general primate pattern, the adoption of cooperative breeding by our hominin ancestors also provides the most parsimonious explanation for the origin of human hyper-cooperation.

Differences in cognitive skills across taxa, and between monkeys and apes in particular, have been explained by different hypotheses, although these often are not supported by systematic interspecific comparisons. Here, we directly compared the cognitive performance of the four great apes and three monkey species (spider monkeys, capuchin monkeys, and long-tailed macaques), differing in their phylogenetic-relatedness and socioecology. We tested subjects on their ability to remember object locations (memory task), track object displacements (transposition task), and obtain out-of-reach rewards (support task). Our results showed no support for an overall clear-cut distinction in cognitive skills between monkeys and apes as species performance varied substantially across tasks. Although we found differences in performance at tracking object displacements between monkeys and apes, interspecific differences in the other two tasks were better explained in terms of differential socioecology, especially differential levels of fission-fusion dynamics. A cluster analysis using mean scores of each condition of the three tasks for each species suggested that the only dichotomy might be between members of the genus Pan and the rest of the tested species. These findings evidence the importance of using multiple tasks across multiple species in a comparative perspective to test different explanations for the enhancement of specific cognitive skills.

Several studies have documented the importance of social bonding for the enhancement of individual fitness. However, little is known about how social relationships develop through ontogeny, and whether their development follows the same trajectory in males and females. Here we analyzed affiliative interactions (proximity, social grooming, play) combined with demographic and genetic data in semi-free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago over their first 4 yr of life (from birth to sexual maturation) to understand how these interactions change through development in both sexes. Generalized linear mixed models revealed that social behaviors mostly followed different developmental trajectories in males and females and were highly dependent on the social context. In particular, sex differences in social behavior varied through development depending on the partner’s sex and age. Females engaged in more social interactions than males, especially with other females, and were more involved in grooming around the time of maturation. In contrast, males interacted more with males and age peers, especially around maturation. Sex differences in social behavior varied through development, but also depended on rank, partner’s rank, and kin line, although not consistently. High-ranking individuals, especially older females, were generally preferred as social partners. Moreover, both male and female individuals interacted mostly with maternal kin, although males also preferred paternal kin over nonkin. Importantly, most developmental changes in sociality happened when individuals were ca. 2 yr old, suggesting that this might be a milestone in the development of sociality in rhesus macaques. The only notable exception to this pattern was play, which was more pronounced in males from the beginning of their lives. We propose that play might serve as a trigger of sex differences in social behavior, with sex differences emerging early in development and increasing through time as males and females gradually grow into their adult social roles.

It has long been debated whether the mind consists of specialized and independently evolving modules, or whether and to what extent a general factor accounts for the variance in performance across different cognitive domains. In this study, we used a hierarchical Bayesian model to re-analyse individual level data collected on seven primate species (chimpanzees, bonobos, orangutans, gorillas, spider monkeys, brown capuchin monkeys and long-tailed macaques) across 17 tasks within four domains (inhibition, memory, transposition and support). Our modelling approach evidenced the existence of both a domain-specific factor and a species factor, each accounting for the same amount (17%) of the observed variance. In contrast, inter-individual differences played a minimal role. These results support the hypothesis that the mind of primates is (at least partially) modular, with domain-specific cognitive skills undergoing different evolutionary pressures in different species in response to specific ecological and social demands.

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Gaze following is an adaptive skill that might have been selected in social species, such as many nonhuman primates, to obtain information about food location, predators, and social interactions. The authors investigated the ability of spider monkeys (Ateles geoffroyi) and capuchin monkeys (Cebus apella) to follow the gaze of a human around barriers and the presence of "looking back" behavior. In the 1st experiment, a human looked to a target location inside the testing room, whereas in the 2nd experiment, the human looked behind an opaque barrier placed outside the testing room. The authors compared the frequency of looking at the target location with the corresponding baseline looking frequencies. Both species (a) showed evidence of spontaneous gaze following in the 1st experiment and (b) engaged in gaze following behind the barrier in the 2nd experiment. In contrast, neither species performed "looking back" responses. The authors conclude that both monkey species showed some indication of perspective-taking abilities, although the absence of "looking back" behavior suggests a potential difference from the abilities shown by the great apes.